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A male-killing gene encoded by a symbiotic virus of Drosophila

Author

Listed:
  • Daisuke Kageyama

    (National Agriculture and Food Research Organization)

  • Toshiyuki Harumoto

    (Kyoto University, Yoshida-honmachi
    Kyoto University, Yoshida-Konoe-cho)

  • Keisuke Nagamine

    (National Agriculture and Food Research Organization)

  • Akiko Fujiwara

    (Gunma University
    RIKEN Center for Sustainable Resource Science)

  • Takafumi N. Sugimoto

    (National Agriculture and Food Research Organization)

  • Akiya Jouraku

    (National Agriculture and Food Research Organization)

  • Masaru Tamura

    (National Institute of Health Sciences)

  • Takehiro K. Katoh

    (Graduate School of Science and Engineering, Ehime University
    Tokyo Metropolitan University)

  • Masayoshi Watada

    (Graduate School of Science and Engineering, Ehime University
    Tokyo Metropolitan University)

Abstract

In most eukaryotes, biparentally inherited nuclear genomes and maternally inherited cytoplasmic genomes have different evolutionary interests. Strongly female-biased sex ratios that are repeatedly observed in various arthropods often result from the male-specific lethality (male-killing) induced by maternally inherited symbiotic bacteria such as Spiroplasma and Wolbachia. However, despite some plausible case reports wherein viruses are raised as male-killers, it is not well understood how viruses, having much smaller genomes than bacteria, are capable of inducing male-killing. Here we show that a maternally inherited double-stranded RNA (dsRNA) virus belonging to the family Partitiviridae (designated DbMKPV1) induces male-killing in Drosophila. DbMKPV1 localizes in the cytoplasm and possesses only four genes, i.e., one gene in each of the four genomic segments (dsRNA1−dsRNA4), in contrast to ca. 1000 or more genes possessed by Spiroplasma or Wolbachia. We also show that a protein (designated PVMKp1; 330 amino acids in size), encoded by a gene on the dsRNA4 segment, is necessary and sufficient for inducing male-killing. Our results imply that male-killing genes can be easily acquired by symbiotic viruses through reassortment and that symbiotic viruses are hidden players in arthropod evolution. We anticipate that host-manipulating genes possessed by symbiotic viruses can be utilized for controlling arthropods.

Suggested Citation

  • Daisuke Kageyama & Toshiyuki Harumoto & Keisuke Nagamine & Akiko Fujiwara & Takafumi N. Sugimoto & Akiya Jouraku & Masaru Tamura & Takehiro K. Katoh & Masayoshi Watada, 2023. "A male-killing gene encoded by a symbiotic virus of Drosophila," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37145-0
    DOI: 10.1038/s41467-023-37145-0
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    References listed on IDEAS

    as
    1. Toshiyuki Harumoto & Bruno Lemaitre, 2018. "Male-killing toxin in a bacterial symbiont of Drosophila," Nature, Nature, vol. 557(7704), pages 252-255, May.
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